Deep-Sea Research I 58 (2011) 273–282

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Deep-Sea Research I

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Prey preferences among the community of deep-diving odontocetes from the Bay of Biscay, Northeast Atlantic

Je´romeˆ Spitz a,b,n, Yves Cherel c, Ste´phane Bertin d, Jeremy Kiszka a, Alexandre Dewez e, Vincent Ridoux a,d a Littoral, Environnement et Socie´te´s, UMR 6250, Universite´ de La Rochelle/CNRS, 2 rue Olympe de Gouges, 17032 La Rochelle, Cedex, France b Parc zoologique de La Fleche, Le Tertre Rouge, 72200 La Fleche, France c Centre d’Etudes Biologiques de Chize´, UPR 1934 du CNRS, BP 14, 79360 Villiers-en-Bois, France d Centre de Recherche sur les Mammiferes Marins, UMS 3419, Universite´ de La Rochelle/CNRS, 17000 La Rochelle, France e Groupe d’Etude de la Faune Marine Atlantique, BP 75, 40130 Capbreton, France article info abstract

Article history: Long-finned pilot whales (Globicephala melas),Risso’sdolphins(Grampus griseus), melon-headed whales Received 14 June 2010 (Peponocephala electra),Cuvier’sbeakedwhales(Ziphius cavirostris), Sowerby’s beaked whales (Mesoplodon Received in revised form bidens), northern bottlenose whales (Hyperoodon ampullatus), sperm whales (Physeter macrocephalus), 14 December 2010 dwarf sperm whales (Kogia sima) and pygmy sperm whales (Kogia breviceps) make up the large Accepted 28 December 2010 community of deep-diving odontocetes occurring off the Bay of Biscay, northeast Atlantic. The ecology Available online 12 January 2011 of these toothed cetaceans is poorly documented worldwide. The present study described their prey Keywords: preferences from stomach content analysis and showed resource partitioning within the assemblage. Marine top predators The majority of the species appeared to be mostly teutophageous. Fish was an important food source Toothed whales only for the Sowerby’s beaked whale and, to a lesser extent, for the long-finned pilot whale. In terms of Cephalopods foraging habitats inferred from prey composition, either pelagic oceanic or demersal neritic habitats Diet Community were exploited by toothed whales in the Bay of Biscay, with only the long-finned pilot whale foraging in Resource partitioning the two habitats. Finally, with more than 14,000 identified cephalopods from 39 species, the present study highlighted also the poorly known deep-sea cephalopod community off the Bay of Biscay using top predators as biological samplers. & 2011 Elsevier Ltd. All rights reserved.

1. Introduction major dimensions: the trophic (prey characteristics), spatial (both on horizontally and vertically) and temporal dimensions (from The diet of a given predator is a combination of resource diel activity patterns to yearly migratory cycles). In marine top availability and foraging strategies. Foraging strategies are con- predator ecology, the study of these dimensions would provide strained by energy requirements and are associated to foraging important advances in the understanding of ecosystem function- costs and benefits. The success of foraging strategies for a predator ing. For example, in the southwest Indian Ocean, the oceanic is linked to limitation in the predator’s physiological, morpholo- island Mayotte is characterized by a high odontocete diversity gical or social functioning. Hence, prey composition in the diet of a (Kiszka et al., 2007a). The existence of resource partitioning given predator results from different evolutionary processes, among co-occurring tropical dolphins around this island was which shaped predator’s characteristics. Since resource partition- revealed by analyzing ecological tracers (carbon and nitrogen ing allows co-existence of predators, inter-specific competition for stable isotopes) from skin and blubber biopsies. Results suggest food is probably a major process in the establishment of different some fine-scale mechanisms of segregation in the species fora- foraging strategies among predators (Roughgarden, 1976). ging habitats and trophic levels (Gross et al., 2009). In the Description of the different dimensions of the ecological niche northeast Atlantic, a broad community of large fish and delphi- allows estimating the degree of overlap versus segregation nids exploits oceanic pelagic ecosystems. Dietary investigations between species (Pianka, 1974). The foraging niche has three highlighted segregating mechanisms along several dimensions of the foraging niche, prey composition, prey size and diurnal activity, and suggested that energy requirements would shape n Corresponding author at: Littoral, Environnement et Socie´te´s, UMR 6250, predator foraging strategies (Pusineri et al., 2008). Universite´ de La Rochelle/CNRS, 2 rue Olympe de Gouges, 17032 La Rochelle, Cedex, France. Tel.: +33 5 46 50 76 58; fax: +33 5 46 44 99 45. The Bay of Biscay in the eastern North Atlantic is a contrasted E-mail address: [email protected] (J. Spitz). marine area with an oceanic domain, a continental slope indented

0967-0637/$ - see front matter & 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr.2010.12.009 274 J. Spitz et al. / Deep-Sea Research I 58 (2011) 273–282 by numerous canyons and a continental shelf, which extends whale (Kogia sima). Secondly, dietary segregation among this com- more than 200 km offshore in the north of the Bay and only 10 km munity of deep-diving odontocetes is investigated using prey char- in the south. The Bay supports a rich cetacean fauna (Hammond acteristics rather than prey taxonomy as descriptors. Finally, this et al., 2002; Kiszka et al., 2007b; Certain et al., 2008). The slope study uses cetaceans as biological samplers for a baseline description and oceanic areas seem to be an important foraging area espe- of the poorly known deep-sea cephalopod fauna in the oceanic Bay of cially for medium to large odontocetes such as the sperm whale Biscay. (Physeter macrocephalus), long-finned pilot whale (Globicephala melas) and a variety of beaked whales (Kiszka et al., 2007b). These toothed whales are often referred to as squid-eating deep-divers 2. Materials and methods but, in general, their ecology is poorly documented around the world. All these species co-occur in the oceanic part of the Bay of 2.1. Sampling Biscay, suggesting some segregation processes within the com- munity. We hypothesized that each species occupies its own Strandings were examined by members of the French strand- foraging niche and that overlap is limited. Therefore, the first aim of ing scheme established since 1972, this monitoring effort this work is the description of prey composition from stomach depends substantially on volunteer involvement. Stranded ani- content analysis of 5 species of medium to large odontocetes: mals were measured, sexed and, after necropsy, stomach contents long-finned pilot whale, Cuvier’s beaked whale (Ziphius cavirostris), were stored deep-frozen (20 1C) in polythene bags until further Sowerby’s beaked whale (Mesoplodon bidens), sperm whale and analyses. pygmy sperm whale (Kogia breviceps). Dietary results are also given A total of 42 stomach contents of adult deep-diving odonto- for 4 additional species for which sample size is low: Risso’s dolphin cetes were collected between 1993 and 2010 (Table 1), including (Grampus griseus), melon-headed whale (Peponocephala electra), 9 species from 4 families (Delphinidae, Ziphiidae, Physeteridae northern bottlenose whale (Hyperoodon ampullatus)anddwarfsperm and Kogiidae): 11 long-finned pilot whales (G. melas), 2 Risso’s

Table 1 Summary of deep-diving odontocetes stranding data in the Bay of Biscay available for dietary analysis.

Species Sexe Length (cm) Date Observers

Long-finned pilot whale Male 258 28 December 1994 CRMM Male 490 18 April 1998 CRMM Male 578 18 April 1999 CRMM Female 295 17 December 1999 CRMM Female 469 13 April 2001 CRMM/J. Vimpere/O. Dian Male 200 4 March 2003 GEFMA Male 371 1 May 2005 CRMM/J. Vimpere Male 540 27 June 2007 CRMM/J. Cloutour Male 596 11 February 2009 ONCFS Male 376 11 March 2009 CRMM Male 211 3 July 1993 GERDAU

Risso’s dolphins Female 170 17 June 1993 GERDAU Female 320 6 May 2009 AL LARK

Melon headed whale Male 243 29 August 2003 CRMM/G. Anselme/J.R. Meslin Male 244 15 October 2008 CRMM/LPO

Cuvier’s beaked whale Male 333 30 November 1998 GEFMA Male 465 30 January 1999 CRMM Female 590 26 November 2002 CRMM/J. Pourreau Male 460 10 January 2007 CRMM/J.J. Boubert/R. Mirtain Male 600 1 March 2007 CRMM/J.R. Meslin/G. Zieback Male 590 31 March 2007 CRMM/GEFMA/G. Gautier Male 540 18 January 2008 CRMM/C. Anselme Female 420 21 January 2008 CRMM/C. Anselme Male 554 7 March 2008 CRMM/ONCFS/J.J. Boubert Female 600 20 April 2008 CRMM/C. Anselme

Sowerby’s beaked whale Male 316 29 May 2007 GEFMA/CRMM Male 370 19 September 2008 CRMM//J.R. Meslin Male 395 20 September 2008 CRMM/O. Dian/J. Cloutour

Northern bottlenose beaked whale Female 610 2 August 2009 G. Gautier/G. Cabassut

Sperm whale Male 1095 23 December 2001 CRMM/GEFMA/MARIN Male 1045 23 December 2001 CRMM/GEFMA/MARIN Male 1050 23 December 2001 CRMM/GEFMA/MARIN

Pygmy sperm whale Female 185 3 February 1984 CRMM Male 225 29 August 1986 CRMM Female 213 30 December 1989 CRMM Male 160 11 December 1990 CRMM Male 275 8 March 1993 CRMM Male 200 7 December 1999 CRMM/J.J. Boubert Male 211 28 December 2001 CRMM Male 167 17 January 2008 CRMM/ONF/ONCFS Male 212 26 August 2010 CRMM/ONF

Dwarf sperm whale Female 175 15 November 1999 CRMM J. Spitz et al. / Deep-Sea Research I 58 (2011) 273–282 275 dolphins (G. griseus), 2 melon-headed whales (P. electra), of prey i found in the diet of predator B. Segregation was considered 10 Cuvier’s beaked whales (Z. cavirostris), 3 Sowerby’s beaked substantial when overlap values were o0.4 (Ross, 1986). whales (M. bidens), 1 northern bottlenose whale (H. ampullatus), The non-parametric Mann–Whitney test was used to compare 3 sperm whales (P. macrocephalus), 1 dwarf sperm whale (K. sima) prey size distributions (significance level of p¼0.05). Calculations and 9 pygmy sperm whales (K. breviceps). For the pygmy sperm- were computed using R software (R Development Core Team, whale, the present work compiles at species-level dietary ana- 2010). Prey characteristics, such as habitat or quality, used to lyses from 7 specimens that were individually published in a describe species foraging strategies were derived from the litera- review paper (Santos et al., 2006), plus data from two recently ture (e.g. Guerra, 1992; Que´ro et al., 2003; Spitz et al., 2010b). stranded individuals.

2.2. Sample analysis 3. Results

Sample analysis followed a general procedure that is now 3.1. Long-finned pilot whale standard for marine top predators (e.g. Cherel et al., 2000; Ridoux, 1994; Spitz et al., 2006). Food remains found in stomachs of The diet was mostly composed of small cephalopods (Table 2). stranded odontocetes were constituted mainly of accumulated A total of 2986 individual prey were found, which accounted for undigested materials. Diagnostic hard parts – fish otoliths and a total reconstructed biomass of about 33 kg. The diet was cephalopod beaks – were sorted from the samples and stored dominated by benthic octopods (% reconstructed biomass 21.1%M, 7 either dry (fish bones and otoliths) or in 70% ethanol (cephalopod estimated mean mantle length 114 16 mm) and the oceanic squids 7 beaks). Food items were identified to the lowest taxonomic level Todarodes sagittatus (17.2%M; 255 78 mm), Histioteuthis reversa 7 by using published guides (Clarke, 1986; Hark¨ onen,¨ 1986; Xavier (10.7%M; 22 11 mm), Histioteuthis bonnellii bonnellii (10.6%M; 7 7 and Cherel, 2009) and our reference collection. The number of 203 29 mm) and Galiteuthis armata (9.2%M; 111 25 mm). Two individuals for each species was estimated from the maximum fish species accounted for a significant part of the diet in terms of number of lower or upper beaks identified for each cephalopod ingested biomass, the conger eel (Conger conger: 8.3%M) and scad species, and from the maximum number of either right or left (Trachurus trachurus: 3.9%M). Finally, salps were occasionally fed otoliths for each fish species. Standard measurements of lower in large quantities (8.1%M). beaks and otoliths were taken using a digital vernier calliper (70.02 mm). A random sub-sample of up to 200 diagnostic hard 3.2. Cuvier’s beaked whale parts per prey species per stomach sample was measured. Cephalopod dorsal mantle length (DML), fish standard length ThedietofCuvier’sbeakedwhalewascomposedofsmallto (SL) and prey body mass were back-calculated by using allometric medium cephalopods, but a few fish and salps remains were also equations (Clarke, 1986; Lu and Ickeringill, 2002; Santos et al., found (Table 2). A total of 5092 individual prey were recovered, 2002; authors’ unpublished data). which accounted for a total reconstructed biomass of about 408 kg. The dietary importance of each prey taxon was described by Cranchiid squids accounted for a third of the reconstructed biomass, its percentages by number (%N) and by reconstructed biomass with include mainly Teuthowenia megalops (22.7%M; 212733 mm) (%M). In this study, the stomach (i.e. the individual predator) was and G. armata (8.0%M; 242724 mm). Another third of reconstituted considered as the sample unit. For each individual, percentage by biomass was composed by histioteuthids, with H. reversa (26.6%M; number and percentage by mass were calculated for each prey 4474 mm) and H. bonnellii bonnellii (4.4%M; 88744 mm). Finally, taxon, and then averaged at predator species-level. Ninety-five the giant octopod Haliphron atlanticus (10%M) and salps (10%M) could per cent confidence intervals (95% CI) around the percentages by occasionally represent significant exploited resources. number and mass were generated for each prey taxon by boot- strap simulations of sampling errors (Santos et al., 2001a). 3.3. Sowerby’s beaked whale The bootstrapping routine was written using the R software (R Development Core Team, 2010). Random samples were drawn Small fish dominated the 294 prey found in the stomach with replacement and the procedure was repeated 1000 times. contents of Sowerby’s beaked whales (Table 2). The total recon- The lower and upper bounds of 95% CI were the 25th and 975th structed biomass was estimated at about 1.6 kg. Four species of values previously ranked in increasing order. gadids were identified, with Micromesistius poutassou (24.7%M; For cetacean species represented by one or two individuals, 155760 mm) and Trisopterus luscus/minutus (13.4%M; 71714 mm) only individual dietary compositions were calculated. being the most important items. The hake Merluccius merluccius was another major fish prey (11.8%M; 111757 mm). The swim- 2.3. Niche segregation ming crabs Polybius spp. (33.0%M) and the cuttlefish species Sepia spp. (8.0%M; 57723 mm) held significant parts of the diet. Niche segregation was only investigated only for 5 species, the long-finned pilot whale, Cuvier’s beaked whale, Sowerby’s beaked 3.4. Sperm whale whale, sperm whale and pygmy sperm whale. Cetacean species represented by one or two individuals were excluded of the analyses. Only cephalopod remains were recovered from the stomachs of Dietary overlaps by number and by mass (O and O , respec- n m sperm whales (Table 2). A total of 6978 individuals were found. tively) within the odontocete assemblage were calculated using They accounted for a total reconstructed biomass of more than the Pianka index, which varies from 0 (no overlap) to 1 (complete 5 tons. With 26 different cephalopod species, the diet of sperm overlap) P whales was highly diversified. However, one species, H. bonnellii piApiB bonnellii, dominated the diet, with about 50% of total reconstructed O ¼ qPffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiP , 2 2 biomass (178737 mm). Another histoteuthid squid, Histioteuthis piA piB arcturii was also a significant prey (11.2%M; 136718 mm). The where piA is the percentage by number or by mass of prey i found in giant octopod H. atlanticus ranked second (18.2%M). Finally, large the diet of predator A and piB is the percentage by number or by mass and giant squids represented a significant part of the diet, with Table 2 276 Diet composition in frequency by number (%N) and reconstructed biomass (%M) of major deep-diving odontocetes in the Bay of Biscay. Confidence intervals at 95% (CI 95%) are given in brackets.

Long-finned pilot whale Cuvier’s beaked whale Sowerby’s beaked whale Pygmy sperm whale Sperm whale

%N (CI 95%) %W (CI 95%) %N (CI 95%) %W (CI 95%) %N (CI 95%) %W (CI 95%) %N (CI 95%) %W (CI 95%) %N (CI 95%) %W (CI 95%)

Cephalopods Sepia spp. 2.9 (0–7.7) 0.6 (0–1.9) 2.8 (0–8.4) 8.0 (0–24.1) Loligo spp. 2.3 (0–5.7) 3.2 (0.2–7.8) 0.3 (0–0.8) 0.5 (0–1.4) Chtenopteryx sicula 0.1 (0–0.1) 0.0 (0–0.1) Ancistrocheirus lesueuri 3.0 (0–9.1) 2.6 (0–7.9) 0.6 (0.1–1.6) 0.4 (0.1–0.9) Octopoteuthis sp. 1.4 (0.8–2) 0.7 (0.3–1) ’’Giant’’ Octopoteuthis 0.1 (0–0.2) 0.2 (0–0.3) Taningia danae 0.3 (0.1–0.7) 5.4 (3.8–8.1) Ancistroteuthis lichtensteini 0.0 (0–0.1) 0.1 (0–0.2) 0.4 (0.1–0.9) 0.2 (0.1–0.5) Moroteuthis/Onykia 0.1 (0–0.1) 0.1 (0–0.1) Cycloteuthis akimushkini 0.2 (0–0.3) 0.3 (0–0.5) Gonatus steenstrupi 0.8 (0–2.3) 1.8 (0–5.4) 2.6 (0.7–4.9) 7.6 (2.3–14.5) 0.6 (0–1.9) 1.5 (0–4.4) 9.4 (0–28) 2.1 (0–6.2) Lepidoteuthis grimaldii 0.7 (0.1–1.2) 3.3 (0.6–5.2)

Pholidoteuthis bochmai 0.1 (0–0.2) 0.3 (0.1–0.5) 273–282 (2011) 58 I Research Deep-Sea / al. et Spitz J. Architeuthis dux 0.3 (0.2–0.3) 6.9 (0.9–16.2) Histioteuthis bonnellii 4.0 (0–10.1) 10.6 (0–25.5) 2.1 (0.5–4.5) 4.4 (0.6–10) 1.5 (0–3.4) 5.5 (0–11.8) 48.5 (42.3–51.7) 48.1 (39.7–63.5) Histioteuthis arcturiii 22.6 (0.1–36.4) 11.2 (0–18.6) Histioteuthis corona 0.3 (0–0.9) 0.7 (0–2.2) Histioteuthis meleagroteuthis 1.5 (0–3.4) 0.9 (0–2) 0.1 (0–0.2) 0.0 (0–0.1) Histioteuthis reversa 12.7 (0.1–34.5) 10.7 (0.4–29.7) 32.6 (13.9–54.6) 26.6 (7.2–50.7) 69.3 (46.5–89) 59.7 (39.9–80.6) 4.7 (4–6.1) 0.4 (0.3–0.5) Brachioteuthis rissei 0.1 (0–0.2) 1.2 (0.5–2.2) 0.1 (0–0.3) 0.6 (0–1.9) 0.1 (0–0.4) Todarodes sagittatus 22.3 (4.5–40.9) 17.2 (4.1–35.8) 2.2 (0.1–5.5) 7.8 (0.2–19.8) 3.5 (0.6–7.7) 9.2 (1.5–18.5) 0.6 (0.4–0.7) 0.4 (0.3–0.5) Und. Ommastrephidae 2.3 (0–5.8) 3.8 (0–10.3) Chiroteuthis veranyi 0.1 (0–0.3) 0.1 (0–0.2) 0.2 (0–0.3) 0.0 (0–0.1) Chiroteuthis sp.1 0.2 (0–0.5) 0.4 (0–1.1) 0.3 (0.1–0.5) 0.0 (0–0.1) Chiroteuthis sp.2 0.2 (0–0.7) 0.9 (0–2.8) Mastigoteuthis A (Imbert) 1.0 (0–3) 0.7 (0–2) 0.0 (0–0.1) 0.0 (0–0.1) 0.3 (0–0.8) 0.1 (0–0.2) Mastigoteuthis schmidti 0.2 (0–0.5) 0.2 (0–0.5) Teutowenia megalops 0.1 (0–0.1) 0.0 (0–0.1) 26.6 (10.9–45.3) 22.7 (9.7–36.3) 0.3 (0–0.8) 0.3 (0–0.7) 2.3 (0.3–5.7) 0.3 (0.1–0.8) Galiteuthis armata 13.7 (0–33.4) 9.2 (0–23) 9.5 (1.4–18.9) 8.0 (1.1–16.5) 0.1 (0–0.1) 0.2 (0–0.6) 4.0 (1.2–8.1) 0.9 (0.2–1.8) Taonius pavo 1.4 (0.2–3.3) 1.2 (0.2–2.6) 0.2 (0–0.7) 0.2 (0–0.5) 0.5 (0–0.9) 0.1 (0–0.1) Megalocranchia sp. 1 1.6 (0.6–2.9) 1.4 (0.4–2.6) 0.6 (0.3–0.7) 0.2 (0.1–0.3) Megalocranchia sp. 2 0.1 (0–0.1) 0.1 (0–0.1) Vampyroteuthis infernalis 0.0 (0–0.1) 0.0 (0–0.1) 0.3 (0–0.8) 0.3 (0–0.8) Und. Octopodidae 14.5 (0.6–32.1) 21.1 (5.3–42) Haliphron atlanticus 10.0 (0–30) 10.0 (0–30) 1.5 (1.4–1.6) 18.2 (12.6–25.5)

Fish Chauliodus sloani 0.1 (0–0.3) 0.1 (0–0.2) Notoscopelus kroeyeri 1.9 (0–5.6) 1.4 (0–4.3) 0.2 (0–0.7) 0.2 (0–0.5) Conger conger 4.5 (0–13.6) 8.3 (0–24.9) Sardina pilchardus 0.6 (0–1.7) 0.6 (0–1.9) Scomber scombrus 0.6 (0–1.7) 0.4 (0–1.2) Micromesistius poutassou 2.30.6 (0–1.7)(0–6.8) 0.20.5 (0–0.6)(0–1.5) 0.1 (0–0.2) 0.1 (0–0.1) 27.420.4 (0–61.1)(0–82.1) 13.424.7 (0–40.3)(0–74.1) 3.5 (0–10.6) 2.8 (0–8.3) GadiculusMerlangius argenteus merlangus 0.13.7 (0–0.4)(0–11.1) 0.17.2 (0–0.3)(0–21.7) 0.9 (0–2.8) 1.1 (0–3.3) TrachurusTrisopterus trachurus spp 4.5 (0–13.6) 3.9 (0–11.6) Merluccius merluccius 0.6 (0–1.7) 0.3 (0–0.8) 2.8 (0–8.4) 11.8 (0–35.3) 0.5 (0–1.4) 0.2 (0–0.7) Fish I 0.1 (0–0.1) – Und. fish 7.7 (0–22.2) –

Others invertebrates Mysids 0.7 (0–2.2) 0.1 (0–0.1) Unid. shrimp 3.8 (0–11.4) 1.0 (0–3.1) Polybius spp. 33.3 (0–100) 33.3 (0–100) 9.0 (0–23.6) 10.5 (0–30.6) Salps 9.1 (0–27.2) 8.1 (0–24.2) 10 (0–30) 10 (0–30) J. Spitz et al. / Deep-Sea Research I 58 (2011) 273–282 277 three important species: Architeuthis dux (6.9%M), Taningia danae 3.7. Niche segregation (5.4%M) and Lepidoteuthis grimaldii (3.3%M). The largest prey belonged to the first species, the giant squid, with an estimated Niche segregation was investigated only for the 5 most docu- dorsal mantle length of 1.5 m for a 46 kg body mass. All other mented species (long-finned pilot whales, Cuvier’s beaked whales, cephalopod species accounted for a much lower fraction of the Sowerby’s beaked whales, sperm whales and pygmy sperm diet by mass. whales). In general, dietary niches were well segregated, showing low values of Pianka’s index in most cases both by number and by 3.5. Pygmy sperm whale mass (Table 4). However, some cases of substantial overlaps were identified. The pygmy sperm whale and the Cuvier’s beaked whale

The diet was mostly composed of small cephalopods, added showed the highest overlap (On¼0.71; Om¼0.68). The diet of with crustaceans and limited amount of fish (Table 2). A total of long-finned pilot whale overlapped slightly in terms of ingested

743 individual preys were found, which accounted for a total biomass composition with the pygmy sperm whale (Om¼0.40) reconstructed biomass of about 27 kg. Despite a large prey and the Cuvier’s beaked whale (Om¼0.39). diversity (18 cephalopods species, 4 fishes and 3 crustaceans), In term of general prey size selection (Fig. 1), the prey body one species, H. reversa, accounted for 59.7%M (36710 mm) of the mass distributions varied significantly between predator species diet. Another histioteuthid squid, H. bonnelli bonnelli, made up a (Mann–Whitney test, po0.05 for each pair-species). The Sower- significant proportion of the diet (5.5%M). The ommastrephid by’s beaked-whale fed almost exclusively on very small prey squid T. sagittatus ranked second in term of cephalopods biomass items (o10 g body mass). The long-finned pilot whale, the with 9.2%M. Finally, the swimming crabs Polybius spp. (33.3%M) pygmy sperm whale and the Cuvier’s beaked whale fed mostly was occasionally exploited. on small prey item (10–100 g body mass) with proportions of very small and medium prey that varied between the different 3.6. Others cetacean species cetaceans. Only sperm whale fed on medium to large preys, with 14% of ingested preys weighting more than 1 kg and the largest The two stomachs of melon-headed whales were both composed prey item being estimated at about 46 kg. When looking at by cephalopods and fish remains (Table 3). Cuttlefish and neritic several of the main prey targeted by odontocetes, G. armata squid species were the dominant cephalopods species. Gadiform (Fig. 2), Gonatus steenstrupi (Fig. 4) and H. bonnelli bonnelli fish, mainly T. luscus/minutus, M. poutassou and M. merluccius were (Fig. 5), length distributions varied significantly between predator identified as important prey for the two melon-headed whales. species (Mann–Whitney test, po0.05). In contrast, size distribu- The first stomach of Risso’s dolphin contained the remains of tions of T. megalops and H. reversa were quite similar across all six cuttlefish (mainly large Sepia officinalis) and one large benthic predators (Figs. 3 and 6). octopod. A small quantity of salps was recovered from the second stomach content (Table 3). The single stomach of dwarf sperm whale contained 44 4. Discussion individuals of H. reversa and remains of one swimming crab Polybius spp. (Table 3). 4.1. Representativeness of dietary results The single stomach of northern bottlenose whale contained 872 cephalopods from two different species that represented Stomach content analysis is subject to some selectivity and biases 86 kg of ingested biomass. The most abundant species by far which could affect our perception of top predator diets. The repre- was the cranchiid T. megalops. The other species was the oceanic sentativeness of diet was in this case subject to difficulty in control- octopod Stauroteuthis syrtensis (Table 3). ling sampling design and to differential digestion of ingested prey

Table 3 Stomach composition in frequency by number (%N) and reconstructed biomass (%M) of additional deep-diving odontocetes in the Bay of Biscay.

Risso’s dolphin Melon headed whale Northern bottlenose Dwarf sperm beaked whale whale

Ind. 1 Ind. 2 Ind. 1 Ind. 2 Ind. 1 Ind. 1

%N %M %N %M %N %M %N %M %N %M %N %M

Cephalopods Sepia spp. 85.7 94.6 35.7 85.6 2.2 24.7 Und. Sepiolidae 19.7 Alloteuthis spp. 7.1 0.6 0.6 0.2 Loligo spp. 7.1 1.8 2.2 13.3 Histioteuthis reversa 97.8 99.6 Und. Ommastrephidae 8.4 37.7 Teutowenia megalops 13.5 93.6 Stauroteuthis syrtensis 86.5 6.4 Und. Octopodidae 14.3 5.4

Fish Micromesistius poutassou 35.7 7.7 Trisopterus spp 58.4 16.5 Merluccius merluccius 14.3 4.3 6.2 5.6 Und. Pleuronectidae 2.2 2.0

Others invertebrates Polybius spp. 2.2 0.4 Salps 100.0 100.0 278 J. Spitz et al. / Deep-Sea Research I 58 (2011) 273–282

Table 4 Niche overlaps (Pianka’s index) in the trophic dimension by number (above diagonal) and by mass (below diagonal). Values in bold denoted substantial overlap (o0.4). Long-finned pilot whale pilot Long-finned Cuvier's beaked whale Sowerby's beaked whale Sperm whale Pygmy sperm whale

Long-finned pilot whale 0.01 0.00 0.17 0.39

Cuvier's beaked whale 0.39 0.00 0.15 0.71

Sowerby's beaked whale 0.00 0.00 0.00 0.00

Sperm whale 0.28 0.12 0.00 0.11

Pygmy sperm whale 0.40 0.68 0.00 0.09

(e.g. Tollit et al., 1997; Santos et al., 2001a; Pierce et al., 2007). Especially for large and/or oceanic species, dietary results are often limited by size, spatio-temporal coverage, or for instance, age, sex, reproductive and health status compositions of individuals providing the stomach content sample set. Thus, several limitations are inherent to small sets of individuals obtained from stranding schemes. Indeed, in our study prey remains were often highly digested and eroded. This was likely a source of biases in quantifying the importance by number and by mass of the different prey species. Species with large diagnostic hard parts were likely overestimated in the diet compared to species having small or no hard parts, because retention time in the stomach would not be the same for all types and sizes of diagnostic parts (e.g. Murie, 1987; Pierce and Boyle, 1991; Santos et al., 2001a). This is particularly relevant for cephalopod beaks which are relatively indigestible and would tend to accumulate in the predators’ stomachs whereas fish bones and otoliths disappear more quickly from stomach contents (Bigg and Fawcett, 1985). Moreover, the number of prey species found in the diet of a top predator increases with the number of analyzed stomachs (Spitz et al., 2006). Hence, diversity of prey species is likely underestimated and confidence limits around the proportion by number and by mass of identified preys are often wide for odontocete species for which only a few stomach samples were analyzed. This study is fully subjected to these limitations and sources of heterogeneity as ontogenetic, temporal or geographic changes cannot be considered here. Nevertheless, published data on dietary preferences of deep-diving cetaceans are scarce and they rely on limited sample sets (see for example, the world review on the diet of beaked whales by MacLeod et al., 2003). Hence, the present work should be considered as providing representative general patterns on prey preferences for the most deep-diving odontocetes of the north- east Atlantic but not as a fine and exhaustive description of their diets.

Fig. 1. Frequency distribution of prey body mass (g) eaten by deep-diving odontocetes in the Bay of Biscay with n¼the number of prey, x7s¼mean value7standard deviation, and [min.max. value]. J. Spitz et al. / Deep-Sea Research I 58 (2011) 273–282 279

Fig. 3. Frequency distributions of LRL (mm) of Teutowenia megalops eaten by deep-diving odontocetes in the Bay of Biscay.

combination of mesopelagic prey living in oceanic waters and of prey living at or close to the bottom in neritic waters. This combination suggested some degree of dietary plasticity allowing long-finned pilot whales to exploit successively both the oceanic and neritic habitats, as previously shown in the Bay of Biscay for only one other cetacean species, the striped dolphin (Stenella coeruleaoalba; Spitz et al., 2006). Secondly, the diet of sperm whales in the northeast Atlantic was dominated either by Gonatus species or by H. bonnellii bonnellii, and the prevalence of one of the two prey species was generally discussed according to migration patterns (Santos et al., 2002). Gonatus, a cold-temperate species, is associated Fig. 2. Frequency distributions of LRL (mm) of Galiteuthis armata eaten by deep- diving odontocetes in the Bay of Biscay. to northern localities such as the North Sea (e.g. Santos et al., 1999, 2002; Simon et al., 2003), whereas H. bonnellii bonnellii was 4.2. Prey preferences described from southern localities such as the Canary Islands (Ferna´ndez et al., 2009) or the Madeira Archipelago (Clarke, Given the limitations discussed above, the present work is 1962). Hence, the vast numbers of H. bonnellii bonnellii and the nevertheless the first quantitative study of prey preferences for a small amount of gonatid squids found in the present work suggest deep-diving assemblage of odontocetes (at least for 5 of the that sperm whales were either foraging in the Bay of Biscay or 9 studied species belonging to 4 families) collected in the same traveling northwards. In the same way, gonatid squids were geographical zone. The key role of cephalopods, mainly oceanic reported as the key prey in the diet of northern bottlenose whales species, was confirmed in the ecology of these deep-diving top across north Atlantic waters (Hooker et al., 2001; Santos et al., predators. Indeed, the majority of studied species appeared to be 2001b). We reported here for the first time the predominance of mostly teutophageous. However, fish seemed to be a significant another squid species, H. reversa, in a stomach content of a northern resource for some species, such as the Sowerby’s beaked whale or bottlenose whale. the long-finned pilot whale. The overall results are consistent Finally, remains of fishing gears, like hooks were recovered with previous studies and they strengthen the already available from two stomach contents of long-finned pilot whales and two albeit scattered data on their feeding habits (e.g. Beatson and of Sowerby’s beaked whales, suggesting that these two species O’shea, 2009; Best, 2007; Blanco et al., 2006; Ferna´ndez et al., may be involved in longline depredation in the Bay of Biscay. 2009; Gannon et al., 1997; Gonzalez et al., 1994; Jefferson and Barros, 1997; MacLeod et al., 2003; Santos et al., 1999, 2001b, c, 4.3. Considerations on cetaceans foraging strategies 2002, 2006; see also references therein). However, the present study highlights some key features. Firstly, the main character- Beyond the taxonomic composition of the diets of these deep- istic of the long-finned pilot whale diet was the unique diving odontocetes, prey biological characteristics can help 280 J. Spitz et al. / Deep-Sea Research I 58 (2011) 273–282

Fig. 5. Frequency distributions of LRL (mm) of Histioteuthis bonnellii bonnellii eaten by deep-diving odontocetes in the Bay of Biscay.

cetaceans seemed be almost exclusively teutophageous. As sea- birds which exhibit different dive behaviors according to whether the prey was a fish, a squid or a crustacean (Elliott et al., 2008), these difference in prey types imply probably different diving strategies among these predators. Similarly, prey size was explored as a possible segregation mechanism within the trophic dimension of the foraging niche. Significant differences occurred between teutophageous predators regarding prey size with pygmy sperm whales feeding on small cephalopods, whereas large species were found in the diet of sperm whales. Difference in Fig. 4. Frequency distributions of LRL (mm) of Gonatus steenstrupi eaten by deep- prey size distribution between toothed whales might reflect two diving odontocetes in the Bay of Biscay. alternative techniques of prey ingestion. The large prey would be captured using pincer-like movement of jaws, whereas small prey documenting indirectly several dimensions of the cetaceans would by ingested by suction-feeding (MacLeod et al., 2006). foraging niche, and so, contribute to a better understanding of Finally, prey quality could be involved in prey selection and segregation mechanisms likely to take place among these pre- trophic segregations among top predators with contrasted energy dators in the Bay of Biscay. requirement (Pusineri et al., 2008; Spitz et al., 2010a). In the Differences were observed along the spatial and trophic dimen- present work, almost all prey species had low energy contents sions of the foraging niche. Indeed, on the axis of foraging habitats, (r4kJg1: Clarke et al., 1985; Spitz et al., 2010b). Hence, diets revealed the presence of both neritic and oceanic prey predator specific energy requirements per unit body mass are assemblages. The continental shelf seabed seemed exclusively interpreted as broadly equivalent across all studied species. exploited by Risso’s dolphins, melon-headed whales and Sowerby’s One possible exception could be the long-finned pilot whale beaked whales, while all other cetaceans exploited mesopelagic whose diet includes several high quality species (Spitz et al., prey living in the oceanic habitat beyond the shelf break, except 2010b) such as scad (T. trachurus), conger eel (C. conger)or long-finned pilot whales that can forage in both habitats. mackerel (Scomber scombrus). Here, high quality preys repre- On the trophic dimension of the foraging niche, three main sented more than 10% of total ingested biomass and were likely prey types, cephalopods, fish and crabs, were recovered in the underestimated as otoliths are less resistant to digestion than present work. Sowerby’s beaked whales was the only species cephalopod beaks. This dietary characteristic of pilot whale would primarily targeting fish, then melon headed whales and long- be consistent with recent telemetry observations of its diving finned pilot whales showed significant part of fish (410%W). behavior. Pilot whales undertake deep foraging sprints, and this Crabs (Polybius spp.) represented a significant part of the diet for costly foraging strategy would be sustainable only if the target Sowerby’s beaked whales and pygmy sperm whales. Others species had a high energy density (Soto et al., 2008). J. Spitz et al. / Deep-Sea Research I 58 (2011) 273–282 281

observed differences in foraging niche among these top marine predators explain their co-existence in the Bay of Biscay.

4.4. Considerations on the cephalopod community

Deep-sea cephalopods are often poorly known all around the world, mainly because of their low value for commercial fisheries and of the difficulties to catch them. Thus, research cruises specifically targeting cephalopods are seldom conducted, and no adapted fishing gears allow adequate sampling of most of species. Nonetheless, cephalopods play an important role in marine food webs, most particularly in deep-sea ecosystems (Rodhouse and Nigmatullin, 1996). In oceanic waters of the northeastern Atlantic, cephalopods constitute a major resource for top predators (e.g. Pusineri et al., 2008; this study). However, the composition of the cephalopod fauna was almost unknown in this area and especially in the oceanic part of the Bay of Biscay. The most detailed, and geographically closest, study described recently the cephalopod fauna along the northern mid-Atlantic ridge from 1295 specimens sampled by trawls (Vecchione et al., 2010). For a better knowledge of cephalopod communities, an alter- native to traditional fishing techniques is the use of top predators as biological samplers (Cherel et al., 2004). Indeed, the diet of top predators can be a good indicator of prey availability and it sometimes brings more data than experimental catches with fishing gears (e.g. Que´ro et al., 2006). In the present study, more than 14,000 individual cephalopods were identified from sto- machs of 9 cetacean species and they shed new insights on the oceanic cephalopod community off the Bay of Biscay. Overall, the cephalopod diversity is fairly high with a least 39 species from 22 families and the presence of charismatic species such as the giant and large squids A. dux, T. danae, L. grimaldii and the ‘‘giant’’ Octopoteuthis, together with the oceanic octopods Vampiroteuthis infernalis and H. atlanticus. Then, the community appears to be dominated by two families, the histioteuthids with the large H. bonnellii bonnellii and the smaller H. reversa, and the cranchiids with mainly T. megalops and G. armata. Thus, the oceanic cepha- lopods community of the Bay of Biscay appears to be different from northern adjacent areas where Gonatus species dominated the cephalopod assemblages (Kristensen, 1984; Vecchione et al., 2010). This study is the first description of the oceanic cephalopod community of the Bay of Biscay. The knowledge of cephalopod biogeography worldwide is decades behind that of other marine taxa (Roeleveld, 1998). Hence, this work brought a valuable new insight on the relative abundance and diversity of oceanic cephalopods living in the northern Atlantic and especially for large species that are almost always absent from trawling surveys.

Acknowledgments

The authors are particularly grateful to members of the French Stranding Scheme and the whole staff of CRMM (Center de Recherche sur les Mammiferes Marins) for providing the samples, to M.B. Santos for her contribution on pygmy sperm whales and her expertise in beak identification, and to M. Berdoulay for Fig. 6. Frequency distributions of LRL (mm) of Histioteuthis reversa eaten by deep- her help on Cuvier’s beaked whale samples. CRMM is funded diving odontocetes in the Bay of Biscay. by Ministere de l’Ecologie et du De´veloppement Durable and by Communaute´ d’Agglome´ration de la Ville de La Rochelle. The Ph.D. In brief, most toothed whales from the Bay of Biscay were thesis of J. Spitz is supported by the Agence Nationale de la segregated by different dimensions of their trophic niche, with Recherche Technique with a CIFRE grant. The authors thank also only pygmy sperm whales showing substantial overlaps with the two reviewers for their helpful comments that greatly both Cuvier’s beaked whales and long-finned pilot whales. These improved the manuscript. 282 J. Spitz et al. / Deep-Sea Research I 58 (2011) 273–282

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